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He graduated from Roosevelt High School in Seattle in 1932, where he began acting in school plays after he was cut from the school basketball team. Thereafter, he worked locally in the theater in Seattle until he entered the United States Army Air Corps during World War II, where he was eventually assigned to their radio service. He announced re-broadcasts prepared for the Armed Forces Radio Service (AFRS). In this role, he served as the announcer for the drama Suspense, dated March 16, 1943.

In addition to his movie roles, Duff also experienced success in television, with appearances in the 1950s series The Star and the Story, Climax! and Crossroads. From January 1957 to July 1958, he appeared with Lupino in the CBS sitcom Mr. Adams and Eve, which revolved around the private lives of two fictitious film stars Howard Adams and Eve Drake. They also served as producers.[10]

Duff had the lead role in the short-lived TV series Dante (which ran for only one season; 1960-61),[10] but found greater success as Detective Sergeant Sam Stone in the ABC police drama Felony Squad (1966-69). Duff appeared in all 73 episodes of the series during its three season run, alongside his co-stars Dennis Cole and Ben Alexander. He also directed one episode; "The Deadly Abductors".[11]

Duff portrayed villain Jules Edwards in Part 1 of the 1981 mini-series East of Eden, and was part of the main cast in the TV series Flamingo Road (1980-82), appearing in all 38 episodes of the show.[13]

He continued to make guest appearances in TV series during the 1980s, including Charlie's Angels (1980) (as bumbling private eye Harrigan in the episode "Harrigan's Angel"); Murder, She Wrote (1984), Magnum, P.I. (1988) (as Capt. Thomas Magnum, II, the grandfather of main character Thomas Magnum, played by Tom Selleck), and Dallas (also 1988).[14] Duff also had a recurring role as Paul Galveston during the sixth season of Knots Landing (1984-85), appearing in 10 episodes. He returned for one more episode in 1990.

After he was listed in Red Channels as a communist subversive in 1950, he lost his radio work and might have forfeited his entire career had it not been for his marriage. Duff and Lupino had a daughter, Bridget Duff (born April 23, 1952). The couple separated in 1966 but did not divorce until 1984. He subsequently married Judy Jenkinson. Like former wife Lupino, Duff was a staunch Democrat.[17]